Abstract
Consumption of meat from animals hunted with Pb ammunition can cause toxic accumulation with consequent health risks, even if relatively small amounts are consumed in each exposure. In El Palmar National Park, Argentina, invasive alien mammals, wild boar (Sus scrofa) and axis deer (Axis axis), are culled with Pb ammunition and their meat is consumed. In this study, we evaluated blood Pb concentrations in 58 consumers of culled game and examined Pb exposure risk according to their demographics, duty, and consumption habits. Likewise, the likelihood of exposure was evaluated by quantifying Pb concentrations in meat samples of seven culled axis deer. Twenty-seven participants (46%) had detectable blood Pb levels (limit of detection = 3.3 μg/dL), with an average 4.75 ± 1.35 μg/dL (geometric mean ± geometric S.D.); the average for all participants was 3.25 ± 1.51 μg/dL. Blood Pb concentrations were significantly higher in hunters, in participants who reported consuming game meat more than 5 times per week, and in participants who reported frequently consuming cured game meat (compared to cooked or pickled). Pb concentration varied significantly along the trajectory of the bullet in deer muscle, being highest at mid-point but with detectable Pb levels even in distant tissue samples (control), suggesting potential for dietary intake by consumers. These findings provide evidence of Pb exposure risk in consumers and emphasize the relevance of replacing Pb ammunition with non-toxic alternatives. This change would reduce dietary exposure in frequent consumers and allow the use of game meat as safe food for people whilst eliminating collateral risks to wild animals and the environment.
Similar content being viewed by others
References
Arnemo JM, Andersen O, Stokke S, Thomas VG, Krone O, Pain DJ, Mateo R (2016) Health and environmental risks from lead-based ammunition: science versus socio-politics. Ecohealth 13:618–622. https://doi.org/10.1007/s10393-016-1177-x
Arrondo E, Navarro J, Perez-García JM, Mateo R, Camarero PR, Martin-Doimeadios RCR, Jiménez-Moreno M, Cortés-Avizanda A, Navas I, García-Fernández AJ, Sánchez-Zapata JA, Donázar JA (2020) Dust and bullets: stable isotopes and GPS tracking disentangle lead sources for a large avian scavenger. Environ Pollut 266:115022. https://doi.org/10.1016/j.envpol.2020.115022
Assi MA, Hezmee MNM, Haron AW et al (2016) The detrimental effects of lead on human and animal health. Vet World 9:660–671. https://doi.org/10.14202/vetworld.2016.660-671
Avery D, Watson T (2009) Regulation of lead-based ammunition around the world. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, Idaho, USA., pp 161–168
Ballari SA, Cirignoli S, Winter M, et al. (2019) Sus scrofa. Categorización 2019 de los mamíferos de Argentina según su riesgo de extinción. Lista Roja de los mamíferos de Argentina. In: SAyDS–SAREM (eds.). http://cma.sarem.org.ar/es/especie-exotica/sus-scrofa. Accessed 28 Dec 1BC
BfR (2011) Lead fragments in game meat can be an added health risk for certain consumer groups. http://www.bfr.bund.de/en/press_information/2011/32/lead_fragments_in_game_meat_can_be_an_added_health_risk_for_certain_consumer_groups-127610.html
Birgisdottir BE, Knutsen HK, Haugen M, Gjelstad IM, Jenssen MTS, Ellingsen DG, Thomassen Y, Alexander J, Meltzer HM, Brantsæter AL (2013) Essential and toxic element concentrations in blood and urine and their associations with diet: Results from a Norwegian population study including high-consumers of seafood and game. Sci Total Environ 463–464:836–844. https://doi.org/10.1016/j.scitotenv.2013.06.078
Bjermo H, Sand S, Nälsén C, Lundh T, Enghardt Barbieri H, Pearson M, Lindroos AK, Jönsson BAG, Barregård L, Darnerud PO (2013) Lead, mercury, and cadmium in blood and their relation to diet among swedish adults. Food Chem Toxicol 57:161–169. https://doi.org/10.1016/j.fct.2013.03.024
Bonnefoy C, Menudier A, Moesch C, Lachâtre G, Mermet JM (2002) Validation of the determination of lead in whole blood by ICP-MS. J Anal At Spectrom 17:1161–1165. https://doi.org/10.1039/b201889f
Broadway MS, McCallen EB, Caudell J, Stewart CM (2020) Ammunition type and shot placement determine lead fragmentation in deer. J Wildl Manag 84:1406–1414. https://doi.org/10.1002/jwmg.21917
Budtz-Jørgensen E, Bellinger DC, Lanphear B, Grandjean P, on behalf of the International Pooled Lead Study Investigators (2013) An international pooled analysis for obtaining a benchmark dose for environmental lead exposure in children. Risk Anal 33:450–461. https://doi.org/10.1111/j.1539-6924.2012.01882.x
Buenz EJ, Parry GJ (2017) Chronic lead intoxication from eating wild-harvested game. Am J Med 131:e181–e184. https://doi.org/10.1016/j.amjmed.2017.11.031
Buenz EJ, Parry GJ, Bauer BA, Matheny LM, Breukel K (2017) A prospective observational study assessing the feasibility of measuring blood lead levels in New Zealand hunters eating meat harvested with lead projectiles. Contemp Clin Trials Commun 5:137–143. https://doi.org/10.1016/j.conctc.2017.02.002
Caldwell KL, Cheng PY, Vance KA, Makhmudov A, Jarrett JM, Caudill SP, Ho DP, Jones RL (2019) LAMP: a CDC program to ensure the quality of blood-lead laboratory measurements. J Public Heal Manag Pract 25:S23–S30. https://doi.org/10.1097/PHH.0000000000000886
Chiodo LM, Covington C, Sokol RJ, Hannigan JH, Jannise J, Ager J, Greenwald M, Delaney-Black V (2007) Blood lead levels and specific attention effects in young children. Neurotoxicol Teratol 29:538–546. https://doi.org/10.1016/j.ntt.2007.04.001
Cindi MD, Mbonane TP, Naicker N (2020) Study protocol to examine the relationship between environmental exposure to lead and blood lead levels among children from day-care centres in Ekurhuleni Metropolitan Municipality. BMJ Open 10:e036687. https://doi.org/10.1136/bmjopen-2019-036687
CLIAwaived.com n.d. https://www.cliawaived.com/amfile/file/download/file/1074/product/3079/
COEH (2016) Prevention of childhood lead toxicity. Pediatrics 138:1. 10.1542/peds.2016-1493
Damerau A, Venäläinen ER, Peltonen K (2012) Heavy metals in meat of Finnish city rabbits. Food Additives and Contaminants: Part B 5(4):246–250. https://doi.org/10.1080/19393210.2012.702131
Dietert RR, Piepenbrink MS (2006) Lead and immune function. Crit Rev Toxicol 36:359–385. https://doi.org/10.1080/10408440500534297
Dobrowolska A, Melosik M (2008) Bullet-derived lead in tissues of the wild boar (Sus scrofa) and red deer (Cervus elaphus). Eur J Wildl Res 54:231–235. https://doi.org/10.1007/s10344-007-0134-y
EFSA Panel on Contaminants in the Food Chain (CONTAM) (2013) Scientific Opinion on Lead in Food. EFSA J 2010 8:4–1570. https://doi.org/10.2903/j.efsa.2010.1570
Fachehoun RC, Lévesque B, Dumas P, St-Louis A, Dubé M, Ayotte P (2015) Lead exposure through consumption of big game meat in Quebec, Canada: risk assessment and perception. Food Addit Contam - Part A Chem Anal Control Expo Risk Assess 32:1501–1511. https://doi.org/10.1080/19440049.2015.1071921
Falandysz J, Szymczyk-Kobrzyńska K, Brzostowski A et al (2005) Concentrations of heavy metals in the tissues of red deer (Cervus elaphus) from the region of Warmia and Mazury, Poland. Food Addit Contam 22:141–149. https://doi.org/10.1080/02652030500047273
Flora SJS, Flora G, Saxena G (2006) Environmental occurrence, health effects and management of lead poisoning. Lead, In, pp 158–228
FSA (2017) Lead-shot game. https://www.food.gov.uk/safety-hygiene/lead-shot-game
García-Fernandez AJ, Jiménez P, María-Mojica P et al (2008) Intoxicacion por plomo en buitres leonados Gyps fulvus. In: Alcantara (ed) Plan de acción para la erradicación del uso ilegal de venenos en el medio natural en Aragón. Actas del Seminario Mortalidad por intoxicación en aves necrófagas. Problemática y soluciones. Ainsa, Huesca (Spain), pp 1–100
Gerofke A, Ulbig E, Martin A, Müller-Graf C, Selhorst T, Gremse C, Spolders M, Schafft H, Heinemeyer G, Greiner M, Lahrssen-Wiederholt M, Hensel A (2018) Lead content in wild game shot with lead or non-lead ammunition – does “state of the art consumer health protection” require non-lead ammunition? PLoS One 13:1–23. https://doi.org/10.1371/journal.pone.0200792
Gerofke A, Martin A, Schlichting D, et al. (2019) Heavy metals in game meat. In: Chemical hazards in foods of animal origin Food safety assurance and veterinary public health. pp 341–366
Green RE, Pain DJ (2015) Risks of health effects to humans in the UK from ammunition-derived lead. In: Delahay RJ, Spray CJ (eds) Proceedings of the Oxford Lead Symposium. Lead ammunition: Understanding and minimising the risks to human and environmental health. The University of Oxford, UK, Edward Grey Institute, p 152
Green RE, Pain DJ (2019) Risks to human health from ammunition-derived lead in Europe. Ambio 48:954–968. https://doi.org/10.1007/s13280-019-01194-x
Grund MD, Cornicelli L, Carlson LT, Butler EA (2010) Bullet fragmentation and lead deposition in white-tailed deer and domestic sheep. Human-Wildlife Interact 4:257–265
Gürtler RE, Martín Izquierdo V, Gil G, Cavicchia M, Maranta A (2017) Coping with wild boar in a conservation area: impacts of a 10-year management control program in north-eastern Argentina. Biol Invasions 19:11–24. https://doi.org/10.1007/s10530-016-1256-5
Gürtler RE, Rodríguez-Planes LI, Gil G, Izquierdo VM, Cavicchia M, Maranta A (2018) Differential long-term impacts of a management control program of axis deer and wild boar in a protected area of north-eastern Argentina. Biol Invasions 20:1431–1447. https://doi.org/10.1007/s10530-017-1635-6
Hampton JO, Laidlaw M, Buenz E, Arnemo JM (2018) Heads in the sand: public health and ecological risks of lead-based bullets for wildlife shooting in Australia. Wildl Res 45:287–306. https://doi.org/10.1071/WR17180
Hunt WG, Burnham W, Parish CN et al (2006) Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc Bull 34:167–170. https://doi.org/10.2193/0091-7648(2006)34[167:bfidri]2.0.co;2
Hunt WG, Watson RT, Oaks JL, Parish CN, Burnham KK, Tucker RL, Belthoff JR, Hart G (2009) Lead bullet fragments in venison from rifle-killed deer: potential for human dietary exposure. PLoS One 4:1–6. https://doi.org/10.1371/journal.pone.0005330
Iqbal S, Blumenthal W, Kennedy C, Yip FY, Pickard S, Flanders WD, Loringer K, Kruger K, Caldwell KL, Jean Brown M (2009) Hunting with lead: association between blood lead levels and wild game consumption. Environ Res 109:952–959. https://doi.org/10.1016/j.envres.2009.08.007
Kanstrup N, Swift J, Stroud DA, Lewis M (2018) Hunting with lead ammunition is not sustainable: European perspectives. Ambio 47:846–857. https://doi.org/10.1007/s13280-018-1042-y
Knott J, Gilbert J, Hoccom DG, Green RE (2010) Implications for wildlife and humans of dietary exposure to lead from fragments of lead rifle bullets in deer shot in the UK. Sci Total Environ 409:95–99. https://doi.org/10.1016/j.scitotenv.2010.08.053
Knutsen HK, Brantsæter AL, Alexander J, Meltzer HM (2015) Associations between consumption of large game animals and blood lead levels in humans in Europe: the Norwegian experience. In: Proceedings of the Oxford Lead Symposium. Lead Ammunition: understanding and minimising the risks to human and environmental health. Edward Grey Institute, The University of Oxford, UK., p 152
Kollander B, Widemo F, Ågren E, Larsen EH, Loeschner K (2017) Detection of lead nanoparticles in game meat by single particle ICP-MS following use of lead-containing bullets. Anal Bioanal Chem 409:1877–1885. https://doi.org/10.1007/s00216-016-0132-6
Kosnett M (2009) Health effects of low dose lead exposure in adults and children, and preventable risk posed by the consumption of game meat harvested with lead ammunition. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans. The Peregrine Fund, Boise, Idaho, USA., pp 24–33
Lambertucci SA, Donázar JA, Huertas AD, Jiménez B, Sáez M, Sanchez-Zapata JA, Hiraldo F (2011) Widening the problem of lead poisoning to a South-American top scavenger: lead concentrations in feathers of wild Andean condors. Biol Conserv 144:1464–1471. https://doi.org/10.1016/j.biocon.2011.01.015
Lanphear BP, Rauch S, Auinger P, Allen RW, Hornung RW (2018) Low-level lead exposure and mortality in US adults: a population-based cohort study. Lancet Public Health 3:e177–e184. https://doi.org/10.1016/S2468-2667(18)30025-2
Legagneux P, Suffice P, Messier JS, Lelievre F, Tremblay JA, Maisonneuve C, Saint-Louis R, Bêty J (2014) High risk of lead contamination for scavengers in an area with high moose hunting success. PLoS One 9:e111546. https://doi.org/10.1371/journal.pone.0111546
Lindboe M, Henrichsen EN, Høgasen HR, Bernhoft A (2012) Lead concentration in meat from lead-killed moose and predicted human exposure using Monte Carlo simulation. Food Addit Contam - Part A Chem Anal Control Expo Risk Assess 29:1052–1057. https://doi.org/10.1080/19440049.2012.680201
Martin A, Müller-Graf C, Selhorst T, Gerofke A, Ulbig E, Gremse C, Greiner M, Lahrssen-Wiederholt M, Hensel A (2019) Comparison of lead levels in edible parts of red deer hunted with lead or non-lead ammunition. Sci Total Environ 653:315–326. https://doi.org/10.1016/j.scitotenv.2018.10.393
Mateo R, Kanstrup N (2019) Regulations on lead ammunition adopted in Europe and evidence of compliance. Ambio 48:989–998. https://doi.org/10.1007/s13280-019-01170-5
Mateo R, Rodríguez-de la Cruz M, Vidal D et al (2007) Transfer of lead from shot pellets to game meat during cooking. Sci Total Environ 372:480–485. https://doi.org/10.1016/j.scitotenv.2006.10.022
Mateo R, Baos AR, Vidal D, Camarero PR, Martinez-Haro M, Taggart MA (2011) Bioaccessibility of pb from ammunition in game meat is affected by cooking treatment. PLoS One 6: https://doi.org/10.1371/journal.pone.0015892
Mathee A, de Jager P, Naidoo S, Naicker N (2017) Exposure to lead in South African shooting ranges. Environ Res 153:93–98. https://doi.org/10.1016/j.envres.2016.11.021
Meltzer HM, Dahl H, Brantsæter AL, Birgisdottir BE, Knutsen HK, Bernhoft A, Oftedal B, Lande US, Alexander J, Haugen M, Ydersbond TA (2013) Consumption of lead-shot cervid meat and blood lead concentrations in a group of adult Norwegians. Environ Res 127:29–39. https://doi.org/10.1016/j.envres.2013.08.007
Menozzi A, Menotta S, Fedrizzi G, Lenti A, Cantoni AM, di Lecce R, Gnudi G, Pérez-López M, Bertini S (2019) Lead and copper in hunted wild boars and radiographic evaluation of bullet fragmentation between ammunitions. Food Addit Contam Part B Surveill 12:182–190. https://doi.org/10.1080/19393210.2019.1588389
Millard S. (2018) EnvStats: an R package for environmental statistics, including US EPA guidance
Müller-graf C, Gerofke A, Martin A, et al. (2017) Reduction of lead contents in game meat: results of the ‘Food safety of game meat obtained through hunting’ research project. In: Game meat hygiene. pp 201–212
Naicker N, de Jager P, Naidoo S, Mathee A (2018) Is there a relationship between lead exposure and aggressive behavior in shooters? Int J Environ Res Public Health 15. https://doi.org/10.3390/ijerph15071427
Neri AJ, Roy J, Jarrett J, Pan Y, Dooyema C, Caldwell K, Umar-Tsafe NT, Olubiyo R, Brown MJ (2014) Analysis of a novel field dilution method for testing samples that exceed the analytic range of point-of-care blood lead analyzers. Int J Environ Health Res 24:418–428. https://doi.org/10.1080/09603123.2013.857390
Ortiz-Ortiz E, García-Nieto E, Juárez-Santacruz L et al (2017) Lead exposure: pottery impact in Tlaxcala, Mexico. Rev Int Contam Ambient 33:57–64. https://doi.org/10.20937/RICA.2017.33.01.05
Palmer CD, Lewis ME, Geraghty CM et al (2006) Determination of lead, cadmium and mercury in blood for assessment of environmental exposure: a comparison between inductively coupled plasma-mass spectrometry and atomic absorption spectrometry. Spectrochim Acta - Part B At Spectrosc 61:980–990. https://doi.org/10.1016/j.sab.2006.09.001
Plaza PI, Uhart M, Caselli A et al (2018) A review of lead contamination in South American birds: The need for more research and policy changes. Perspect Ecol Conserv:1–7. https://doi.org/10.1016/j.pecon.2018.08.001
Romano M, Ferreyra H, Ferreyroa G, Molina FV, Caselli A, Barberis I, Beldoménico P, Uhart M (2016) Lead pollution from waterfowl hunting in wetlands and rice fields in Argentina. Sci Total Environ 545–546:104–113. https://doi.org/10.1016/j.scitotenv.2015.12.075
Sevillano Morales J, Moreno-Ortega A, Amaro Lopez MA, Arenas Casas A, Cámara-Martos F, Moreno-Rojas R (2018) Game meat consumption by hunters and their relatives: a probabilistic approach. Food Addit Contam - Part A Chem Anal Control Expo Risk Assess 35:1739–1748. https://doi.org/10.1080/19440049.2018.1488183
Slabe VA, Anderson JT, Cooper J, Miller TA, Brown B, Wrona A, Ortiz P, Buchweitz J, McRuer D, Dominguez-Villegas E, Behmke S, Katzner T (2020) Feeding ecology drives lead exposure of facultative and obligate avian scavengers in the eastern United States. Environ Toxicol Chem 39:882–892. https://doi.org/10.1002/etc.4680
SNFA (2012) Lead in game in Sweden. https://www.bfr.bund.de/cm/343/lead-in-game-in-sweden.pdf
Sobin C, Parisi N, Schaub T, de la Riva E (2011) A Bland-Altman comparison of the Lead Care® System and inductively coupled plasma mass spectrometry for detecting low-level lead in child whole blood samples. J Med Toxicol 7:24–32. https://doi.org/10.1007/s13181-010-0113-7
Stanton NV, Fritsch T (2007) Evaluation of a second-generation portable blood lead analyzer in an occupational setting. Am J Ind Med 50:1018–1024. https://doi.org/10.1002/ajim.20525
Stewart CM, Veverka NB (2011) The extent of lead fragmentation observed in deer culled by sharpshooting. J Wildl Manag 75:1462–1466. https://doi.org/10.1002/jwmg.174
Stokke S, Brainerd S, Arnemo JM (2017) Metal deposition of copper and lead bullets in moose harvested in Fennoscandia. Wildl Soc Bull 41:98–106. https://doi.org/10.1002/wsb.731
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Molecular, clinical and environmental toxicology Volume 3: Environmental Toxicology. Mol Clin Environ Toxicol 101:133–164. https://doi.org/10.1007/978-3-7643-8340-4
Tekindal MA, Erdoğan BD, Yavuz Y (2017) Evaluating left-censored data through substitution, parametric, semi-parametric, and nonparametric methods: a simulation study. Interdiscip Sci Comput Life Sci 9:153–172. https://doi.org/10.1007/s12539-015-0132-9
Thomas VG (2019) Rationale for the regulated transition to non-lead products in Canada: a policy discussion paper. Sci Total Environ 649:839–845. https://doi.org/10.1016/j.scitotenv.2018.08.363
Thomas VG, Pain DJ, Kanstrup N, Green RE (2020) Setting maximum levels for lead in game meat in EC regulations: An adjunct to replacement of lead ammunition. Ambio. 49:2026–2037. https://doi.org/10.1007/s13280-020-01336-6
Tsuji LJS, Wainman BC, Jayasinghe RK, VanSpronsen EP, Liberda EN (2009) Determining tissue-lead levels in large game mammals harvested with lead bullets: human health concerns. Bull Environ Contam Toxicol 82:435–439. https://doi.org/10.1007/s00128-009-9647-2
Uhart M, del Ferreyra HV, Romano M et al (2019) Lead pollution from hunting ammunition in Argentina and current state of lead shot replacement efforts. Ambio 48:1015–1022. https://doi.org/10.1007/s13280-019-01178-x
Wennberg M, Lundh T, Sommar JN, Bergdahl IA (2015) Time trends and exposure determinants of lead and cadmium in the adult population of northern Sweden 1990–2014. Environ Res 159:111–117. https://doi.org/10.1016/j.envres.2017.07.029
WHO (2010) Exposure to lead: a major public health concern. World Health Organization, Geneva
WHO (2019) Lead poisoning and health. https://www.who.int/news-room/fact-sheets/detail/lead-poisoning-and-health. Accessed 28 Dec 1BC
WHO (2020) Brief guide to analytical methods for measuring lead in blood, second edition. World Health Organization, Geneva
Wiemeyer GM, Pérez MA, Torres Bianchini L, Sampietro L, Bravo GF, Jácome NL, Astore V, Lambertucci SA (2017) Repeated conservation threats across the Americas: high levels of blood and bone lead in the Andean Condor widen the problem to a continental scale. Environ Pollut 220:672–679. https://doi.org/10.1016/j.envpol.2016.10.025
Wright JP, Dietrich KN, Ris MD, Hornung RW, Wessel SD, Lanphear BP, Ho M, Rae MN (2008) Association of prenatal and childhood blood lead concentrations with criminal arrests in early adulthood. PLoS Med 5:0732–0739. https://doi.org/10.1371/journal.pmed.0050101
Zowczak M, Niedziałek G, Miler R, et al. (2016) The concentration of lead in muscle tissue of wild boars (Sus scrofa) in selected voivodeships in Poland.
Acknowledgements
We thank G. Wiemeyer for lending the LeadCare® II device, and S. Barandiaran and J. Uhart for logistical support. Special thanks are due to El Palmar National Park (EPNP) staff, especially L. Loyza, J. Yone, E. Munich, J. Zermathen, R. Achilli, J. Ballay, E. Bouvet, I. Ovelar, D. Lugreen, E Perrón, M. Panziera, M. Cardoso, and A. Maranta. We are also thankful to J.M. Hervás, C. Lipuma, and E. Ochoa, EPNP managers. We thank members of the Conservación Tierra de Palmares hunting club and the independent hunters group. We are grateful to those who voluntarily enrolled in the study and to San Benjamín Public Hospital staff, especially the biochemists, vaccinators, and radiologists. We acknowledge Administración de Parques Nacionales for launching Pb ammunition replacement for alien species control in 2019 and the Programa de Conservación Comunitaria del Territorio (UNICEN) for promoting wildlife conservation and human well-being through a One Health approach. We thank volunteers C. Villalba, M. Bartolotta, P. Ferrer, A. Aguiar, B. Resler, E. Amatte, M. Funes, and M. Guerrero. We are especially grateful to WWW Foundation and Secretaría de Políticas Universitarias (Ministerio de Educación, Cultura, Ciencia y Tecnología, Argentina) for funding this work. Delegación Centro-Este de la Administración de Parques Nacionales provided research permits (IF-2019-46151534-APN-DNC # APNAC).
Availability of data and materials
Supporting data and materials will be made available online upon acceptance at https://zenodo.org
Funding
The study on its data collection phase was funded by WWW Foundation and Secretaría de Políticas Universitarias del Ministerio de Educación, Cultura, Ciencia y Tecnología, Argentina (reference number 105/19, Expte. 2018-14465730).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by AEC, AT, WEC, VF, RETV, and MMU. The first draft of the manuscript was written by MMU, AT, and VF, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
All procedures performed in this study involving human participants were in accordance with the ethical standards of the Argentinean National Research Committee (Central Committee of Bioethics in Practice and Biomedical Research of the city of Paraná, Entre Ríos province, reference number 2312401) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.
Consent for publication
Informed consent was obtained from all individual participants included in the study.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tammone, A., Caselli, A.E., Condorí, W.E. et al. Lead exposure in consumers of culled invasive alien mammals in El Palmar National Park, Argentina. Environ Sci Pollut Res 28, 42432–42443 (2021). https://doi.org/10.1007/s11356-021-13654-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-13654-7